Ribonucleotide reductase subunit p53R2 regulates mitochondria homeostasis and function in KB and PC-3 cancer cells

Biochemical and Biophysical Research Communications

Volumn 410, Issue 1, 2011, Pages 102-107

  Wang, Xiaochen ^a,b   Liu, Xiyong ^b   Xue, Lijun ^b   Zhang, Keqiang ^b   Kuo, Mei Ling ^b   Hu, Shuya ^b   Zhou, Bingsen ^b   Ann, David ^b   Zhang, Suzhan ^a   Yen, Yun ^b  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

ATP synthesis; Cytochrome c oxidase; Membrane potential; Mitochondrial DNA (mtDNA) synthesis; P53R2 (RRM2B)

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RIBONUCLEOTIDE REDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CELL FUNCTION; CELL ORGANELLE; CLINICAL EXAMINATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; EVIDENCE BASED PRACTICE; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN TISSUE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; HOMEOSTASIS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NEOPLASMS; RIBONUCLEOTIDE REDUCTASES;

EID: 79959378002     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.05.114     Document Type: Article

References (31)

1. Nordlund P., Reichard P. Ribonucleotide reductases. Annu. Rev. Biochem. 2006, 75:681-706.
2. Tanaka H., Arakawa H., Yamaguchi T., Shiraishi K., Fukuda S., Matsui K., et al. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 2000, 404:42-49.
3. Cooperman B.S., Kashlan O.B. A comprehensive model for the allosteric regulation of Class Ia ribonucleotide reductases. Adv. Enzyme Regul. 2003, 43:167-182.
4. Cory J.G., Sato A. Regulation of ribonucleotide reductase activity in mammalian cells. Mol. Cell. Biochem. 1983, 53-54:257-266.
5. Wright J.A., Chan A.K., Choy B.K., Hurta R.A., McClarty G.A., Tagger A.Y. Regulation and drug resistance mechanisms of mammalian ribonucleotide reductase, and the significance to DNA synthesis. Biochem. Cell Biol., Biochimie et biologie cellulaire 1990, 68:1364-1371.
6. Guittet O., Hakansson P., Voevodskaya N., Fridd S., Graslund A., Arakawa H., et al. Mammalian p53R2 protein forms an active ribonucleotide reductase in vitro with the R1 protein, which is expressed both in resting cells in response to DNA damage and in proliferating cells. J. Biol. Chem. 2001, 276:40647-40651.
7. Kimura T., Takeda S., Sagiya Y., Gotoh M., Nakamura Y., Arakawa H. Impaired function of p53R2 in Rrm2b-null mice causes severe renal failure through attenuation of dNTP pools. Nat. Genet. 2003, 34:440-445.
8. Bourdon A., Minai L., Serre V., Jais J.P., Sarzi E., Aubert S., et al. Mutation of RRM2B, encoding p53-controlled ribonucleotide reductase (p53R2), causes severe mitochondrial DNA depletion. Nat. Genet. 2007, 39:776-780.
9. Zhang K., Hu S., Wu J., Chen L., Lu J., Wang X., et al. Overexpression of RRM2 decreases thrombspondin-1, increases VEGF production in human cancer cells in vitro, in vivo: implication of RRM2 in angiogenesis. Mol. Cancer 2009, 8:11.
10. Zhou B., Liu X., Mo X., Xue L., Darwish D., Qiu W., et al. The human ribonucleotide reductase subunit hRRM2 complements p53R2 in response to UV-induced DNA repair in cells with mutant p53. Cancer Res. 2003, 63:6583-6594.
11. Spinazzola A., Viscomi C., Fernandez-Vizarra E., Carrara F., D'Adamo P., Calvo S., et al. MPV17 encodes an inner mitochondrial membrane protein and is mutated in infantile hepatic mitochondrial DNA depletion. Nat. Genet. 2006, 38:570-575.
12. Zindy F., Eischen C.M., Randle D.H., Kamijo T., Cleveland J.L., Sherr C.J., et al. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 1998, 12:2424-2433.
13. Yen Y., Grill S.P., Dutschman G.E., Chang C.N., Zhou B.S., Cheng Y.C. Characterization of a hydroxyurea-resistant human KB cell line with supersensitivity to 6-thioguanine. Cancer Res. 1994, 54:3686-3691.
14. Zhou B.S., Ker R., Ho R., Yu J., Zhao Y.R., Shih J., et al. Determination of deoxyribonucleoside triphosphate pool sizes in ribonucleotide reductase cDNA transfected human KB cells. Biochem. Pharmacol. 1998, 55:1657-1665.
15. Xue L., Zhou B., Liu X., Wang T., Shih J., Qi C., et al. Structurally dependent redox property of ribonucleotide reductase subunit p53R2. Cancer Res. 2006, 66:1900-1905.
16. Smiley S.T., Reers M., Mottola-Hartshorn C., Lin M., Chen A., Smith T.W., et al. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Natl Acad. Sci. USA 1991, 88:3671-3675.
17. Sastre J., Pallardo F.V., Vina J. The role of mitochondrial oxidative stress in aging. Free Radic. Biol. Med. 2003, 35:1-8.
18. Lebedeva M.A., Eaton J.S., Shadel G.S. Loss of p53 causes mitochondrial DNA depletion and altered mitochondrial reactive oxygen species homeostasis. Biochim. Biophys. Acta 2009, 1787:328-334.
19. Hakansson P., Hofer A., Thelander L. Regulation of mammalian ribonucleotide reduction and dNTP pools after DNA damage and in resting cells. J. Biol. Chem. 2006, 281:7834-7841.
20. Pontarin G., Ferraro P., Hakansson P., Thelander L., Reichard P., Bianchi V. P53R2-dependent ribonucleotide reduction provides deoxyribonucleotides in quiescent human fibroblasts in the absence of induced DNA damage. J. Biol. Chem. 2007, 282:16820-16828.
21. Thelander L. Ribonucleotide reductase and mitochondrial DNA synthesis. Nat. Genet. 2007, 39:703-704.
22. Pontarin G., Gallinaro L., Ferraro P., Reichard P., Bianchi V. Origins of mitochondrial thymidine triphosphate: dynamic relations to cytosolic pools. Proc. Natl Acad. Sci. USA 2003, 100:12159-12164.
23. Ylikallio E., Page J.L., Xu X., Lampinen M., Bepler G., Ide T., et al. Ribonucleotide reductase is not limiting for mitochondrial DNA copy number in mice. Nucleic Acids Res 2010, 38:8208-8218.
24. Chang L., Zhou B., Hu S., Guo R., Liu X., Jones S.N., et al. ATM-mediated serine 72 phosphorylation stabilizes ribonucleotide reductase small subunit p53R2 protein against MDM2 to DNA damage. Proc. Natl Acad. Sci. USA 2008, 105:18519-18524.
25. Xue L., Zhou B., Liu X., Heung Y., Chau J., Chu E., et al. Ribonucleotide reductase small subunit p53R2 facilitates p21 induction of G1 arrest under UV irradiation. Cancer Res. 2007, 67:16-21.
26. Schraufstatter I.U., Hyslop P.A., Hinshaw D.B., Spragg R.G., Sklar L.A., Cochrane C.G. Hydrogen peroxide-induced injury of cells and its prevention by inhibitors of poly(ADP-ribose) polymerase. Proc. Natl. Acad. Sci. USA 1986, 4908-4912.
27. Polyak K., Li Y., Zhu H., Lengauer C., Willson J.K., Markowitz S.D., et al. Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat. Genet. 1998, 20:291-293.
28. Clayton D.A., Vinograd J. Complex mitochondrial DNA in leukemic and normal human myeloid cells. Proc. Natl Acad. Sci. USA 1969, 62:1077-1084.
29. Parrella P., Xiao Y., Fliss M., Sanchez-Cespedes M., Mazzarelli P., Rinaldi M., et al. Detection of mitochondrial DNA mutations in primary breast cancer and fine-needle aspirates. Cancer Res. 2001, 61:7623-7626.
30. Liu V.W., Shi H.H., Cheung A.N., Chiu P.M., Leung T.W., Nagley P., et al. High incidence of somatic mitochondrial DNA mutations in human ovarian carcinomas. Cancer Res. 2001, 61:5998-6001.
31. Xue L., Zhou B., Liu X., Qiu W., Jin Z., Yen Y. Wild-type p53 regulates human ribonucleotide reductase by protein-protein interaction with p53R2 as well as hRRM2 subunits. Cancer Res. 2003, 63:980-986.